diff --git a/zio-http/src/main/scala/zio/http/Route.scala b/zio-http/src/main/scala/zio/http/Route.scala
index ec1994e453..4592f923c7 100644
--- a/zio-http/src/main/scala/zio/http/Route.scala
+++ b/zio-http/src/main/scala/zio/http/Route.scala
@@ -216,6 +216,13 @@ sealed trait Route[-Env, +Err] { self =>
    */
   def routePattern: RoutePattern[_]
 
+  /**
+   * Applies the route to the specified request. The route must be defined for
+   * the request, or else this method will fail fatally.
+   */
+  final def run(request: Request)(implicit trace: Trace): ZIO[Env, Either[Err, Response], Response] =
+    Routes(self).run(request)
+
   /**
    * Returns a route that automatically translates all failures into responses,
    * using best-effort heuristics to determine the appropriate HTTP status code,
diff --git a/zio-http/src/main/scala/zio/http/Routes.scala b/zio-http/src/main/scala/zio/http/Routes.scala
index d6e60d0ca1..a13d4f8117 100644
--- a/zio-http/src/main/scala/zio/http/Routes.scala
+++ b/zio-http/src/main/scala/zio/http/Routes.scala
@@ -127,6 +127,40 @@ final class Routes[-Env, +Err] private (val routes: Chunk[zio.http.Route[Env, Er
   def provideEnvironment(env: ZEnvironment[Env]): Routes[Any, Err] =
     new Routes(routes.map(_.provideEnvironment(env)))
 
+  def run(request: Request)(implicit trace: Trace): ZIO[Env, Either[Err, Response], Response] = {
+
+    class RouteFailure[+Err](val err: Cause[Err]) extends Throwable(null, null, true, false) {
+      override def getMessage: String = err.unified.headOption.fold("<unknown>")(_.message)
+
+      override def getStackTrace(): Array[StackTraceElement] =
+        err.unified.headOption.fold[Chunk[StackTraceElement]](Chunk.empty)(_.trace).toArray
+
+      override def getCause(): Throwable =
+        err.find { case Cause.Die(throwable, _) => throwable }
+          .orElse(err.find { case Cause.Fail(value: Throwable, _) => value })
+          .orNull
+
+      def fillSuppressed()(implicit unsafe: Unsafe): Unit =
+        if (getSuppressed().length == 0) {
+          err.unified.iterator.drop(1).foreach(unified => addSuppressed(unified.toThrowable))
+        }
+
+      override def toString =
+        err.prettyPrint
+    }
+    var routeFailure: RouteFailure[Err] = null
+
+    handleErrorCauseZIO { cause =>
+      routeFailure = new RouteFailure(cause)
+      ZIO.refailCause(Cause.die(routeFailure))
+    }
+      .apply(request)
+      .mapErrorCause {
+        case Cause.Die(value: RouteFailure[_], _) if value == routeFailure => routeFailure.err.map(Left(_))
+        case cause                                                         => cause.map(Right(_))
+      }
+  }
+
   /**
    * Returns new routes that automatically translate all failures into
    * responses, using best-effort heuristics to determine the appropriate HTTP